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Virologica Sinica logoLink to Virologica Sinica
. 2014 Nov 14;29(6):364–371. doi: 10.1007/s12250-014-3507-x

Viral respiratory infections among Hajj pilgrims in 2013

Osamah Barasheed 1,, Harunor Rashid 1, Mohammad Alfelali 1,2, Mohamed Tashani 1, Mohammad Azeem 1, Hamid Bokhary 3, Nadeen Kalantan 4, Jamil Samkari 2, Leon Heron 1, Jen Kok 5, Janette Taylor 5, Haitham El Bashir 6, Ziad A Memish 7, Elizabeth Haworth 8, Edward C Holmes 9,10, Dominic E Dwyer 5,9, Atif Asghar 3, Robert Booy 1,9,10; Hajj Research Team
PMCID: PMC7090649  PMID: 25413828

Abstract

Middle East respiratory syndrome coronavirus (MERS-CoV) has emerged in the Arabian Gulf region, with its epicentre in Saudi Arabia, the host of the ‘Hajj’ which is the world’s the largest mass gathering. Transmission of MERS-CoV at such an event could lead to its rapid worldwide dissemination. Therefore, we studied the frequency of viruses causing influenza-like illnesses (ILI) among participants in a randomised controlled trial at the Hajj 2013. We recruited 1038 pilgrims from Saudi Arabia, Australia and Qatar during the first day of Hajj and followed them closely for four days. A nasal swab was collected from each pilgrim who developed ILI. Respiratory viruses were detected using multiplex RT-PCR. ILI occurred in 112/1038 (11%) pilgrims. Their mean age was 35 years, 49 (44%) were male and 35 (31%) had received the influenza vaccine pre-Hajj. Forty two (38%) pilgrims had laboratory-confirmed viral infections; 28 (25%) rhinovirus, 5 (4%) influenza A, 2 (2%) adenovirus, 2 (2%) human coronavirus OC43/229E, 2 (2%) parainfluenza virus 3, 1 (1%) parainfluenza virus 1, and 2 (2%) dual infections. No MERS-CoV was detected in any sample. Rhinovirus was the commonest cause of ILI among Hajj pilgrims in 2013. Infection control and appropriate vaccination are necessary to prevent transmission of respiratory viruses at Hajj and other mass gatherings.

Keywords: Hajj, influenza-like illness, mass gathering, MERS-CoV, pilgrim, respiratory infections

Footnotes

Hajj Research Team: [Ibtihal Malawi, Ebtehal Matar, Abrar Tawakoul, Abrar ALnami, Atheer Alshareif, Israa Kalantan, Asal Arbaeen, Eatimad Alalawi, Afnan AlGhamdi, Amani Koshak, Ameerah Alkhaldi, Enasm Al-Nami, Anwar Howsawi, Bashaier Fairaq, Bushra Maghrabi, Tafaol Murad, Hanan Alzahrani, Kholood Almehmadi, Doaa Milibari, Rehab Hafiz, Rawdhah Kalantan, Shahad Al-Ansari, Aeshah Rajab, Anood Alfahmy, Ghaida Ali, Fatimah Abu naji, Lujin Hassan, Lulwah Althumali, Layla Farhat, Najlaa Baddour, Hibh Alandanusi, Waad Alqurashi, Sumayyah Fallata, Azhar Alharbi, Joud Bahakeem, Abrar Alshareef, Badr Rawa, Daniah Alnemari, Mawadah Hariri, Samah Alhadramy, Ahmed Alghamdi, Ahmed Muqadimi, Ahmad Bimah, Osama Alamri, Jehad Qutub, Abdulrahman Al-Ghamdi, Abdurrahman Mirza, Abdulghafur Alandijani, Omar Qoqandi, Faisal Mandourah, Muhammad Alghamdi, Mohammed Mahboob, Mohannad Alsulami, Moayyd Hinnawi, Naif Hawsawi, Mousab Alsudais, Nawaf Dhabab, Ahmed Balamash, Mohammed Bawazir, Raif Nassir, Mohammed AlAsmari, Faisal Alzahrani, Abdulrahman Alomari and Ahmad Makeen]

References

  1. Al-Tawfiq J A, Memish Z A. Emerging respiratory viral infections: MERS-CoV and influenza. Lancet Respir Med. 2014;2:23–25. doi: 10.1016/S2213-2600(13)70255-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alborzi A, Aelami M H, Ziyaeyan M, Jamalidoust M, Moeini M, Pourabbas B, Abbasian A. Viral etiology of acute respiratory infections among Iranian Hajj pilgrims, 2006. J Travel Med. 2009;16:239–242. doi: 10.1111/j.1708-8305.2009.00301.x. [DOI] [PubMed] [Google Scholar]
  3. Alghamdi I G, Hussain II, Almalki S S, Alghamdi M S, Alghamdi M M, El-Sheemy M A. The pattern of Middle East respiratory syndrome coronavirus in Saudi Arabia: a descriptive epidemiological analysis of data from the Saudi Ministry of Health. Int J Gen Med. 2014;7:417–423. doi: 10.2147/IJGM.S67061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Askling H H, Rombo L. Influenza in travellers. Curr Opin Infect Dis. 2010;23:421–425. doi: 10.1097/QCO.0b013e32833c6863. [DOI] [PubMed] [Google Scholar]
  5. Barasheed O, Badahdah A-M, Heron L, Taylor J, McPhee K, Ridda I, Haworth E, Dwyer D E, Rashid H, Booy R, Onbehalf of the Hajj Research T Pilot randomised controlled trial to test effectiveness of facemasks in preventing influenza-like illness transmission among Australian Hajj pilgrims in 2011. Infect Disord Drug Targets. 2014;14:110–116. doi: 10.2174/1871526514666141021112855. [DOI] [PubMed] [Google Scholar]
  6. Belderok S M, Rimmelzwaan G F, van den Hoek A, Sonder G J. Effect of travel on influenza epidemiology. Emerg Infect Dis. 2013;20:1821–1827. doi: 10.3201/eid1906.111864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benkouiten S, Charrel R, Belhouchat K, Drali T, Nougairede A, Salez N, Memish Z A, AL Masri M, Fournier P-E, Raoult D, Brouqui P, Parola P, Gautret P. Emerg Infect Dis. 2014. Respiratory Viruses and Bacteria among Pilgrims during the 2013 Hajj. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Benkouiten S, Gautret P, Belhouchat K, Drali T, Nougairede A, Salez N, Memish Z A, Al Masri M, Raoult D, Brouqui P, Parola P, Charrel R N. Comparison of nasal swabs with throat swabs for the detection of respiratory viruses by real-time reverse transcriptase PCR in adult Hajj pilgrims. J Infect. 2014;20:1821–1827. doi: 10.1016/j.jinf.2014.08.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Benkouiten S, Charrel R, Belhouchat K, Drali T, Salez N, Nougairede A, Zandotti C, Memish Z A, Al Masri M, Gaillard C, Parola P, Brouqui P, Gautret P. Circulation of respiratory viruses among pilgrims during the 2012 Hajj pilgrimage. Clin Infect Dis. 2013;57:992–1000. doi: 10.1093/cid/cit446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bialek S R, Allen D, Alvarado-Ramy F, Arthur R, Balajee A, Bell D, Best S, Blackmore C, Breakwell L, Cannons A, Brown C, Cetron M, Chea N, Chommanard C, Cohen N, Conover C, Crespo A, Creviston J, Curns A T, Dahl R, Dearth S, DeMaria A, Echols F, Erdman D D, Feikin D, Frias M, Gerber SI, Gulati R, Hale C, Haynes L M, Heberlein-Larson L, Holton K, Ijaz K, Kapoor M, Kohl K, Kuhar D T, Kumar A M, Kundich M, Lippold S, Liu L, Lovchik J C, Madoff L, Martell S, Matthews S, Moore J, Murray L R, Onofrey S, Pallansch M A, Pesik N, Pham H, Pillai S, Pontones P, Pringle K, Pritchard S, Rasmussen S, Richards S, Sandoval M, Schneider E, Schuchat A, Sheedy K, Sherin K, Swerdlow D L, Tappero J W, Vernon M O, Watkins S, Watson J, Centers for Disease ControlPrevention CDC First confirmed cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in the United States, updated information on the epidemiology of MERS-CoV infection, and guidance for the public, clinicians, and public health authorities-May 2014. MMWR Morb Mortal Wkly Rep. 2014;63:431–436. [PMC free article] [PubMed] [Google Scholar]
  11. Blyth C C, Foo H, van Hal S J, Hurt A C, Barr I G, McPhie K, Armstrong P K, Rawlinson W D, Sheppeard V, Conaty S, Staff M, Dwyer D E. Influenza outbreaks during World Youth Day 2008 mass gathering. Emerg Infect Dis. 2010;16:809–815. doi: 10.3201/eid1605.091136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Corman V M, Muller M A, Costabel U, Timm J, Binger T, Meyer B, Kreher P, Lattwein E, Eschbach-Bludau M, Nitsche A, Bleicker T, Landt O, Schweiger B, Drexler J F, Osterhaus A D, Haagmans B L, Dittmer U, Bonin F, Wolff T, Drosten C. 2012. Assays for laboratory confirmation of novel human coronavirus (hCoV-EMC) infections. Euro Surveill, 17. [DOI] [PubMed]
  13. Davis X M, Hay K A, Plier D A, Chaves S S, Lim P L, Caumes E, Castelli F, Kozarsky P E, Cetron M S, Freedman D O. International travelers as sentinels for sustained influenza transmission during the 2009 influenza A (H1N1) pdm09 pandemic. J Travel Med. 2013;20:177–184. doi: 10.1111/jtm.12025. [DOI] [PubMed] [Google Scholar]
  14. Deris Z Z, Hasan H, Sulaiman S A, Wahab M S, Naing N N, Othman N H. The prevalence of acute respiratory symptoms and role of protective measures among Malaysian hajj pilgrims. J Travel Med. 2010;17:82–88. doi: 10.1111/j.1708-8305.2009.00384.x. [DOI] [PubMed] [Google Scholar]
  15. Devi J P, Noraini W, Norhayati R, Kheong C C, Badrul A, Zainah S, Fadzilah K, Hirman I, Hakim S L, Hisham A N. Laboratory-confirmed case of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in Malaysia: preparedness and response, April 2014. Euro Surveill. 2014;19.pii:20797. doi: 10.2807/1560-7917.es2014.19.18.20797. [DOI] [PubMed] [Google Scholar]
  16. Gaunt E R, Hardie A, Claas E C, Simmonds P, Templeton K E. Epidemiology and clinical presentations of the four human coronaviruses 229E, HKU1, NL63, and OC43 detected over 3 years using a novel multiplex real-time PCR method. J Clin Microbiol. 2010;48:2940–2947. doi: 10.1128/JCM.00636-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gautret P, Vu Hai V, Sani S, Doutchi M, Parola P, Brouqui P. Protective measures against acute respiratory symptoms in French pilgrims participating in the Hajj of 2009. J Travel Med. 2011;18:53–55. doi: 10.1111/j.1708-8305.2010.00480.x. [DOI] [PubMed] [Google Scholar]
  18. Gautret P, Charrel R, Benkouiten S, Belhouchat K, Nougairede A, Drali T, Salez N, Memish Z A, Al Masri M, Lagier J C, Million M, Raoult D, Brouqui P, Parola P. Lack of MERS coronavirus but prevalence of influenza virus in French pilgrims after 2013 Hajj. Emerg Infect Dis. 2014;20:728–730. doi: 10.3201/eid2004.131708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hameed A A, Habeeballah T. Curr World Environ. 2013. Air Microbial Contamination at the Holly Mosque, Makkah, Saudi Arabia; p. 8. [Google Scholar]
  20. Haworth E, Barasheed O, Memish Z A, Rashid H, Booy R. Prevention of influenza at Hajj: applications for mass gatherings. J R Soc Med. 2013;106:215–223. doi: 10.1258/jrsm.2012.120170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Health Protection Agency HPA UK Novel Coronavirus Investigation team. Evidence of person-to-person transmission within a family cluster of novel coronavirus infections, United Kingdom, 2013. Euro Surveill. 2013;18:20427. doi: 10.2807/ese.18.11.20427-en. [DOI] [PubMed] [Google Scholar]
  22. Jaureguiberry S, Boutolleau D, Grandsire E, Kofman T, Deback C, Ait-Arkoub Z, Bricaire F, Agut H, Caumes E. Clinical and microbiological evaluation of travel-associated respiratory tract infections in travelers returning from countries affected by pandemic A(H1N1) 2009 influenza. J Travel Med. 2012;19:22–27. doi: 10.1111/j.1708-8305.2011.00570.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Memish Z A, Assiri A M, Hussain R, Alomar I, Stephens G. Detection of respiratory viruses among pilgrims in Saudi Arabia during the time of a declared influenza A(H1N1) pandemic. J Travel Med. 2012;19:15–21. doi: 10.1111/j.1708-8305.2011.00575.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Memish Z A, Al Rabeeah A A. Health conditions for travellers to Saudi Arabia for the Umra and pilgrimage to Mecca (Hajj) — 2014. J Epidemiol Glob Health. 2014;4:73–75. doi: 10.1016/j.jegh.2014.02.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Memish Z A, Assiri A, Almasri M, Alhakeem R F, Turkestani A, Al Rabeeah A A, Al-Tawfiq J A, Alzahrani A, Azhar E, Makhdoom H Q. Prevalence of MERS-CoV nasal carriage and compliance with the Saudi health recommendations among pilgrims attending the 2013 Hajj. J Infect Dis. 2014;210:1067–1072. doi: 10.1093/infdis/jiu150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Memish Z A, Al-Tawfiq J A, Makhdoom H Q, Assiri A, Alhakeem R F, Albarrak A, Alsubaie S, Al-Rabeeah A A, Hajomar W H, Hussain R, Kheyami A M, Almutairi A, Azhar E I, Drosten C, Watson S J, Kellam P, Cotten M, Zumla A. Respiratory tract samples, viral load, and genome fraction yield in patients with Middle East respiratory syndrome. J Infect Dis. 2014;210:1590–1594. doi: 10.1093/infdis/jiu292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Raoult D, Charrel R, Gautret P, Parola P. From the Hajj: it’s the flu, idiot. Clin Microbiol Infect. 2014;20:O1. doi: 10.1111/1469-0691.12448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rashid H, Barasheed O, Booy R. Acute febrile respiratory infection symptoms in Australian Hajjis at risk of exposure to Middle East respiratory syndrome coronavirus. Med J Aust. 2013;199:453. doi: 10.5694/mja13.10984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rashid H, Azeem M I, Heron L, Haworth E, Booy R, Memish Z A. Has Hajj-associated Middle East Respiratory Syndrome Coronavirus transmission occurred? The case for effective post-Hajj surveillance for infection. Clin Microbiol Infect. 2014;20:273–276. doi: 10.1111/1469-0691.12492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rashid H, Shafi S, Haworth E, El Bashir H, Memish Z A, Sudhanva M, Smith M, Auburn H, Booy R. Viral respiratory infections at the Hajj: comparison between UK and Saudi pilgrims. Clin Microbiol. 2008;14:569–574. doi: 10.1111/j.1469-0691.2008.01987.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rashid H, Shafi S, Booy R, El Bashir H, Ali K, Zambon M, Memish Z, Ellis J, Coen P, Haworth E. Influenza and respiratory syncytial virus infections in British Hajj pilgrims. Emerg Health Threats J. 2008;1:e2. doi: 10.3134/ehtj.08.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ratnamohan V M, Taylor J, Zeng F, McPhie K, Blyth C C, Adamson S, Kok J, Dwyer D E. Pandemic clinical case definitions are non-specific: multiple respiratory viruses circulating in the early phases of the 2009 influenza pandemic in New South Wales, Australia. Virol J. 2014;11:113. doi: 10.1186/1743-422X-11-113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tsiodras S, Baka A, Mentis A, Iliopoulos D, Dedoukou X, Papamavrou G, Karadima S, Emmanouil M, Kossyvakis A, Spanakis N, Pavli A, Maltezou H, Karageorgou A, Spala G, Pitiriga V, Kosmas E, Tsiagklis S, Gkatzias S, Koulouris N, Koutsoukou A, Bakakos P, Markozanhs E, Dionellis G, Pontikis K, Rovina N, Kyriakopoulou M, Efstathiou P, Papadimitriou T, Kremastinou J, Tsakris A, Saroglou G. A case of imported Middle East Respiratory Syndrome coronavirus infection and public health response, Greece, April 2014. Euro Surveill. 2014;19:20782. doi: 10.2807/1560-7917.es2014.19.16.20782. [DOI] [PubMed] [Google Scholar]
  34. Walker E, Ison M G. Respiratory viral infections among hospitalized adults: experience of a single tertiary healthcare hospital. Influenza Other Respir Viruses. 2014;8:282–292. doi: 10.1111/irv.12237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wang M, Barasheed O, Rashid H, Booy R, El Bashir H, Haworth E, Ridda I, Holmes E C, Dwyer D E, Nguyen-Van-Tam J, Memish Z A, Heron L. J Epidemiol Glob Health. 2014. A cluster-randomised controlled trial to test the effectiveness of facemasks in preventing respiratory virus infection among Hajj pilgrims. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zepeda-Lopez H M, Perea-Araujo L, Miliar-Garcia A, Dominguez-Lopez A, Xoconostle-Cazarez B, Lara-Padilla E, Ramirez Hernandez J A, Sevilla-Reyes E, Orozco M E, Ahued-Ortega A, Villasenor-Ruiz I, Garcia-Cavazos R J, Teran L M. Inside the outbreak of the 2009 influenza A (H1N1)v virus in Mexico. PLoS One. 2010;5:e13256. doi: 10.1371/journal.pone.0013256. [DOI] [PMC free article] [PubMed] [Google Scholar]

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